Impact of habitat loss on the diversity and structure of ecological networks between oxyurid nematodes and spur-thighed tortoises (Testudo graecaL.)

Abstract

Habitat loss and fragmentation are recognized as affecting the nature of biotic interactions, although we still know little about such changes for reptilian herbivores and their hindgut nematodes, in which endosymbiont interactions could range from mutualistic to commensal and parasitic. We investigated the potential cost and benefit of endosymbiont interactions between the spur-thighed tortoise (Testudo graeca L.) and adult oxyurid nematodes (Pharyngodonidae order Oxyurida) in scrublands of southern Spain. For this, we assessed the association between richness and abundance of oxyurid species with tortoises’ growth rates and body traits (weight and carapace length) across levels of habitat loss (low, intermediate and high). Furthermore, by using an intrapopulation ecological network approach, we evaluated the structure and diversity of tortoise–oxyurid interactions by focusing on oxyurid species infesting individual tortoises with different body traits and growth rates across habitats. Overall, tortoise body traits were not related to oxyurid infestation across habitats. Oxyurid richness and abundance however, showed contrasting relationships with growth rates across levels of habitat loss. At low habitat loss, oxyurid infestation was positively associated with growth rates (suggesting a mutualistic oxyurid–tortoise relationship), but the association became negative at high habitat loss (suggesting a parasitic relationship). Furthermore, no relationship was observed when habitat loss was intermediate (suggesting a commensal relationship). The network analysis showed that the oxyurid community was not randomly assembled but significantly nested, revealing a structured pattern for all levels of habitat loss. The diversity of interactions was lowest at low habitat loss. The intermediate level, however, showed the greatest specialization, which indicates that individuals were infested by fewer oxyurids in this landscape, whereas at high habitat loss individuals were the most generalized hosts. Related to the latter, connectance was greatest at high habitat loss, reflecting a more uniform spread of interactions among oxyurid species. At an individual level, heavier and larger tortoises tended to show a greater number of oxyurid species interactions. We conclude that there is an association between habitat loss and the tortoise–oxyurid interaction. Although we cannot infer causality in their association, we hypothesize that such oxyurids could have negative, neutral and positive consequences for tortoise growth rates. Ecological network analysis can help in the understanding of the nature of such changes in tortoise–oxyurid interactions by showing how generalized or specialized such interactions are under different environmental conditions and how vulnerable endosymbiont interactions might be to further habitat loss.

Implications for Conservation of Collection of Mediterranean Spur-Thighed Tortoise as Pets in Morocco: Residents’ Perceptions, Habits, and Knowledge

“…In our study, tortoise owners rarely make use of available sources of information (e.g., books, the Internet, or a vet's assessment) to familiarize themselves with the species' habits and requirements, which may explain their limited knowledge of the species. This scarcity of owners' knowledge regarding a basic understanding of their pets and their welfare has also been observed in studies developed in the USA and Canada with other pet reptile species [42,[57][58][59]. In our study, most people did not know about tortoises' reproduction habits, and even acknowledged difficulties in identifying the gender of the tortoise kept at home.…”

“…Injuries are usually reported in the case of tortoises that share homes with dogs or from garden machines as a result of tortoise hiding behavior. Diseases might be expected in tortoises kept as pets as it has been reported elsewhere in this tortoise species; a mutualistic relationship such as nematode-tortoise, often turns to a parasitic relationship harming the tortoise body condition [59]. The isolation or the continuous presence of a possible predator like dogs might cause fear, anxiety, and distress on the tortoises, regarding the rarity of living in a flat-very different from their natural environment- [60] and the continuous feeling of being susceptible of being preyed.…”

Prevalence and intensity of gastrointestinal parasites in the vulnerable spur-thighed tortoise (<em>Testudo graeca</em>) from the central-western of Morocco

“…In addition to the agriculture which characterizes SKF, overgrazing by goats and camels (Karmaoui, 2016) constitute pressure on the vegetation in the site, which leads to a scarcity of feeding resources (Barje et al, 2005). In this context, Benítez-Malvido et al, (2019) suggested that in a low habitat loss, oxyurid infection was positively associated with growth rates, suggesting a mutualistic relationship. This association became negative at high habitat loss, suggesting a parasitic relationship.…”

“…The high prevalence of oxyurids could be explained by their commensal relationship with the host (Roca, 1999;Gagno, 2005). Oxyurid infections are generally suggested to have a beneficial effect in digestion and assimilation of plants, preventing constipation in herbivorous reptile hosts (Rataj et al, 2011;Benítez-Malvido et al, 2019). Moreover, the oxyurid nematodes manifest low pathogenic effects on parasitized tortoises (Traversa et al, 2005;Chávarri et al, 2012).…”

“…However, information on tortoise-gastrointestinal parasite interactions is very scanty, while the parasitism is recognized as a fundamental factor naturally driving the dynamics of animal populations (Fournié et al, 2015). In Spain, Benítez-Malvido et al, (2019), highlighting the relationship between nematode parasites richness and abundance with growth rates of T. graeca across levels of habitat loss. In Morocco, the rare studies performed on gastrointestinal parasites of this vulnerable species concerned the systematic description (Bouamer et al, 2001a;2001b;Bouamer & Morand, 2005).…”